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Towards a Complete Generic-Level Plastid Phylogeny of the Paleotropical Woody Bamboos (Poaceae: Bambusoideae)

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Towards a Complete Generic-Level Plastid Phylogeny of the Paleotropical Woody Bamboos (Poaceae: Bambusoideae) TAXON 66 (3) • June 2017: 539–553 Zhou & al. • Phylogeny of paleotropical woody bamboos (Poaceae) SYSTEMATICS AND PHYLOGENY Towards a complete generic-level plastid phylogeny of the paleotropical woody bamboos (Poaceae: Bambusoideae) Meng-Yuan Zhou,1,4 Yu-Xiao Zhang,1,2 Thomas Haevermans3 & De-Zhu Li1,2,4 1 Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China 2 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China 3 Muséum National d’Histoire Naturelle, Département Systématique et Evolution, Unité Mixte de Recherche 7205 CNRS/MNHN Origine Structure et Evolution de la Biodiversité, Case postale 39, 57 rue Cuvier, 75231 Paris Cedex 05, France 4 Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan 650201, China Author for correspondence: De-Zhu Li, [email protected] ORCID DZL, http://orcid.org/0000-0002-4990-724X DOI https://doi.org/10.12705/663.2 Abstract Paleotropical woody bamboos (PWB) are phylogenetically and taxonomically intractable. Because previous stud- ies included deficient samples or lacked informative characters for tree construction, phylogenetic relationships within the PWB remain incompletely resolved. This study presents the most extensively sampled phylogeny of the PWB with 18 plastid regions and a sample of 144 (35%) ingroup species representing 40 (85%) genera and 8 outgroup species. Results confirmed Melocanninae as the earliest diverging lineage from the rest of the group, and Hickeliinae (including Nastus s.str.) and Racemobambosinae are separately placed within the PWB. Bambusinae is phylogenetically heterogeneous and consists of the Dinochloa-Greslania-Mullerochloa-Neololeba-Sphaeroambos (DGMNS) assemblage, Temburongia simplex, and the core Bambusinae. The core Bambusinae may be redefined to include a basal grade, which contains Kinabaluchloa, Holttumochloa, Bonia, Neomicrocalamus, Temochloa, Soejatmia and an unidentified taxon, and the Bambusa-Dendrocalamus-Gigantochloa (BDG) complex. The BDG complex is extremely diverse in morphology and is subdivided into six subclades. Within the Melocanninae, Davidsea, Neohouzeaua and Ochlandra are closely related to Schizostachyum. Phylogenetic relationships are mostly supported by morphological and geographical evidence. In addition, novel interpretations are provided in the re- delimitation of some taxa. Keywords molecular phylogeny; Paleotropics; phylogenetic relationship; plastid regions; woody bamboos Supplementary Material The Electronic Supplement (Tables S1 & S2; Figs. S1–S5) is available in the Supplementary Data section of the online version of this article at http://ingentaconnect.com/content/iapt/tax; data matrices are available from TreeBASE (http://purl.org/phylo/treebase/phylows/study/TB2:S19282) INTRODUCTION been identified. Furthermore, the PWB are a group of bamboos that remain taxonomically difficult because of their morpho- Woody bamboos are of high economic, cultural and eco- logical variation (Li & al., 2006). Consequently, their taxonomy logical value, and include the most genera and species in the has always been controversial (Electr. Suppl.: Table S1A, B). Bambusoideae (Poaceae). They are widely distributed on all The most updated tribal and subtribal classification of major landmasses except Antarctica and Europe (Li, 1998; bamboos recognizes four subtribes in the PWB: Bambusinae Judziewicz & al., 1999; Ohrnberger, 1999; BPG [Bamboo J.Presl, Melocanninae Benth., Racemobambosinae Stapleton Phylogeny Group], 2012). Much remains to be explored regard- and Hickeliinae A.Camus (BPG, 2012; Soreng & al., 2015). ing their taxonomy and phylogeny. The paleotropical woody Phylogenetic analyses based on both plastid and nuclear DNA bamboos (PWB) consist of 47 genera and ca. 407 species with a sequence data indicate that Melocanninae is monophyletic, and distribution in tropical and subtropical areas of Asia, Africa and plastid data suggest its early divergence from the remaining Oceania (Soderstrom & Ellis, 1987; Dransfield & Widjaja, 1995; PWB (Yang & al., 2007, 2008; Sungkaew & al., 2009; Goh & Ohrnberger, 1999; BPG, 2012; Soreng & al., 2015). Although al., 2013). The long, hollow, stiff and steeple-like appendage the monophyly of PWB received strong statistical support in on the apex of the ovary is a good criterion for Melocanninae analyses of plastid data, a morphological synapomorphy has not species to be distinguished from other subtribes, whereas the Received: 27 Jun 2016 | returned for (first) revision: 8 Nov 2016 | (last) revision received: 23 Feb 2017 | accepted: 23 Feb 2017 || publication date(s): online fast track, n/a; in print and online issues, 23 Jun 2017 || © International Association for Plant Taxonomy (IAPT) 2017 Version of Record 539 Zhou & al. • Phylogeny of paleotropical woody bamboos (Poaceae) TAXON 66 (3) • June 2017: 539–553 top of the ovary in other species is usually broadly conical, solid regions used can influence the topology and support value of and hairy (Holttum, 1956; Yang & al., 2008). In contrast, rela- trees. Therefore, a thorough study with extensive sampling tionships among the other three subtribes remain unresolved covering all four subtribes of the PWB is needed. Plastid se- (Kelchner & BPG, 2013). quences have long been used in phylogenetic reconstruction of Several studies have been conducted on the phylogeny of plants, including bamboos. As the plastomes are uniparentally certain subtribes of PWB. In subtribe Melocanninae, four gen- inherited, much effort has been made to explore the usage of era, Melocanna Trin., Pseudostachyum Munro, Schizostachyum nuclear sequences, including genomic data. Still, in the woody Nees and Cephalostachyum Munro, correspond to clades (Yang bamboos, usage of nuclear or ribosomal nuclear sequences have & al., 2007, 2008). Morphological characters also support the been limited to GBSSI, LEAFY and ITS, and topologies are delimitation of the four subclades. In contrast, Hickeliinae and generally incongruent between plastid and nuclear phylogenies Racemobambosinae are poorly studied possibly because of the (Guo & al., 2002; Guo & Li, 2004; Yang & al., 2008; Yang & narrow geographical distribution of Hickeliinae and because al., 2010; Goh & al., 2013; Yang & al., 2013). Because of the Racemobambosinae contains only one genus. Recently, sub- allohexaploidy of the PWB which causes further difficulties tribal status of Racemobambosinae has been supported by a in identifying single-copy orthologous genes (Triplett & al., phylogenetic study in which two species of Racemobambos 2014), reconstruction of plastid phylogenetic framework is an Holttum were sampled (Goh & al., 2013). In contrast, the initial and indispensable step to our understanding of the com- monophyly of subtribe Hickeliinae has not been supported plex evolutionary history of the woody bamboos, including by six plastid regions (Chokthaweepanich, 2014). Apart from hybridization and allopolyploidization. Here, we (1) provide Melocanninae, Bambusinae is the most studied subtribe of the an overall understanding of phylogenetic relationships among PWB. Goh & al. (2013) recovered four distinct lineages: (1) the the PWB by including a large sample of taxa of the PWB to Bambusa-Dendrocalamus-Gigantochloa (BDG) complex, (2) generate a plastid phylogeny; (2) investigate phylogenetic rela- the Holttumochloa-Kinabaluchloa clade, (3) the Dinochloa- tionships among and within major clades with an emphasis on Mullerochloa-Neololeba-Sphaerobambos (DMNS) clade and the Melocanninae and the Bambusinae clades; and (3) investi- (4) Temburongia simplex S.Dransf. & K.M.Wong. The BDG gate the phylogenetic positions of insufficiently studied genera complex appears to be the most phylogenetically complex such as Davidsea Soderstr. & R.P.Ellis, Greslania Balansa, group of the PWB, probably because of incomplete lineage Nastus Juss., Neohouzeaua A.Camus, Ochlandra Thwaites, sorting and introgressive hybridization (Goh & al., 2013). The Oreobambos K.Schum. and Temochloa S.Dransf. three genera Bambusa Schreb., Dendrocalamus Nees and Gigantochloa Kurz ex Munro were not recovered as mono- phyletic. Furthermore, none of the six subgenera of Bambusa MATERIALS AND METHODS and Dendrocalamus have been supported as monophyletic by molecular phylogenetic studies (Yang & al., 2008; Goh & Taxon sampling. — Subtribe and genus nomenclature fol- al., 2010; Yang & al., 2010). Neomicrocalamus Keng f., Bonia lows BPG (2012), whereas species nomenclature for the Chinese Balansa, Melocalamus Benth. and Thyrsostachys Gamble were taxa follows that in Flora of China (FoC; Li & al., 2006). We each recovered as monophyletic (Yang & al., 2008; Yang & al., include three additional Chinese species not recorded in FoC 2010). Results from Yang & al. (2008) recovered a sister-clade (e.g., McClure, 1940; Wen, 1991). relationship between Neomicrocalamus and Bonia. Taxon sampling encompasses 144 (35%) species of 40 Because the PWB are widely distributed geographically, (85%) genera of the PWB covering their geographic distri- and because most genera have a relatively concentrated dis- butions and morphological diversity (Table 1). The missing tribution in certain areas, phylogenetic studies have been genera are Dendrochloa C.E.Parkinson, Fimbri bambusa restricted to local geographic areas, e.g., bamboos of the Widjaja, Hitchcockella A.Camus,
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